Distinct topographic-anatomical patterns in primary and secondary brain tumors and their therapeutic potential

Abstract

Purpose Understanding the topographic-anatomical patterns of brain tumors has the potential to improve our pathophysiological understanding and may allow for anatomical tailoring of surgery and radiotherapy. This study analyzed topographic-anatomical patterns underlying neuroepithelial tumors, primary CNS lymphoma and metastases. Methods Any histologically confirmed supra- or infratentorial parenchymal neoplasia of one institution over a 4-year period was included. Using high-resolution magnetic resonance imaging data, a detailed analysis of the topographic-anatomical tumor features was performed. Differences between neuroepithelial tumors, primary central nervous system lymphoma (PCNSL) and metastases were assessed using pairwise comparisons adjusted for multiple testing, upon significance of the omnibus test. Results Based on image analysis of 648 patients—419 (65%) neuroepithelial tumors, 28 (5%) PCNSL and 201 (31%) metastases—entity-specific topographic-anatomical patterns were identified. Neuroepithelial tumors showed a radial ventriculo-cortical orientation, inconsistent with the current belief of a growth along white matter tracts, whereas the pattern in PCNSL corresponded to a growth along such. Metastases preferentially affected the cortex and subcortical white matter of large arteries’ terminal supply areas. This study provides a comprehensive anatomical description of the topography of NT, PCNSL and metastases intended to serve as a topographic reference for clinicians and neuroscientists. Conclusions The identified distinct anatomical patterns provide evidence for a specific interaction between tumor and anatomical structures, following a pathoclitic concept. Understanding differences in their anatomical behavior has the potential to improve our pathophysiological understanding and to tailor therapy of brain tumors. Electronic supplementary material The online version of this article (10.1007/s11060-020-03574-w) contains supplementary material, which is available to authorized users.

Topographic brain tumor anatomy drives seizure risk and enables machine learning based prediction

“…The dependence on histopathology only consists of metastases as negative driver and astrocytoma as well as WHO grade I as positive drivers. A plausible explanation is the unequal prevalence of the different tumor types with predominance of glioblastoma, metastases and astrocytoma ( Akeret et al, 2020 , Siegel et al, 2020 ). Certain cerebellar structures, such as the cerebellar subcortical white matter and the inferior semilunar/gracile lobules influence the prediction in the direction of “seizures”.…”

“…However, assuming a causal relationship would be a wrong conclusion, as the inference analysis provided strong evidence against it. The fact that a subcortical cerebellar location in the inferior semilunar/gracile lobule is the most frequent manifestation of cerebellar metastases ( Akeret et al, 2020 ) might be an explanation for the dependence of the model on these variables. The associated risk of concomitant supratentorial metastases and thus an increased risk of seizures might create this dependence.…”

“…The classification of anatomical brain tumor features followed a predefined segmentation scheme ( Akeret et al, 2020 ), described in Supplementary Table 2 and illustrated in Supplementary Fig. 1 .…”

The Infratentorial Localization of Brain Metastases May Correlate with Specific Clinical Characteristics and Portend Worse Outcomes Based on Voxel-Wise Mapping

“…More importantly, analyses mapping the distribution of BMs were conducted using MRI voxel-based methods, and certain associations between BMs locations and primary malignancies were found. The preferred localization of BMs at the grey-white matter junction and the watershed regions had been well documented, which was explained by the trapping of tumor emboli in the terminal supply areas of large intracranial arteries [ 9 , 10 , 11 ]. Further investigations regarding voxel-based landscapes of BM sites similarly demonstrated that the posterior fossa was a predilection watershed site of BMs from lung and breast cancers [ 10 , 12 , 13 , 14 , 15 ].…”

Topographic volume-standardization atlas of the human brain

“…Specific anatomical patterns are seen for example in inflammatory conditions such as amyotrophic lateral sclerosis (Bede et al 2016) or autoimmune encephalitis (Dalmau and Graus 2018). Different brain tumors show distinct topographic anatomical patterns (Akeret et al 2020). The brain also exhibits an anatomically selective vulnerability to metabolic disease (Patel 1994) or toxic injury (Valk and van der Knaap 1992).…”